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Type: Article
Published: 2023-03-15
Page range: 68-81
Abstract views: 214
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Contribution to the knowledge of the genus Boucheona (Oligochaeta, Hormogastridae) in France with a newly described species and a redescribed species

1Department of Biodiversity, Ecology and Evolution, Faculty of Biology, Univerisdad Complutense de Madrid, Madrid, Spain.
1Department of Biodiversity, Ecology and Evolution, Faculty of Biology, Univerisdad Complutense de Madrid, Madrid, Spain.
2Grupo de Ecoloxía Animal (GEA), Universidade de Vigo, E-36310 Vigo, Spain.
1Department of Biodiversity, Ecology and Evolution, Faculty of Biology, Univerisdad Complutense de Madrid, Madrid, Spain.
3 CEFE, Univ Montpellier, CNRS, EPHE, IRD, Montpellier, France.
Annelida Earthworms alpha taxonomy integrative systematics biogeography soil diversity

Abstract

Hormogastrid earthworms are found in the diversity hotspot of the Franco-Iberian domain, together with the better-known family Lumbricidae. Integrative systematics (the combination of morphological, molecular and ecological data) have increased our knowledge of the diversity and evolutionary history of these earthworms, highlighting unresolved taxonomic conflicts. One example of a species group in need of integrative taxonomic revision is the genus Boucheona in France. In this work, we analyzed their diversity using previously published data together with additional data obtained from recently sampled localities. Molecular data including DNA barcodes and additional markers enabled us to reconstruct Bayesian and time-calibrated phylogenies to discuss the evolutionary relationships among the different taxa, and to propose hypotheses regarding their biogeographical history. Based on our results, four species of Boucheona are present in Southern France, including two new taxa. Morphological distinctness and molecular phylogenetics results supported the status of four populations as the newly described Boucheona corbierensis sp. nov., as well as the status of “Hormogaster pretiosa var. nigra” as an independent species, redescribed as Boucheona tenebrae sp. nov. These results provide a new perspective of the importance of the genus Boucheona in southern France, as the possible evolutionary origin of a clade of giant anecic earthworms with unknown (but probably remarkable) impact on ecosystem functioning across their range.

 

References

  1. Akaike, H. (1973) Information theory and an extension of the maximum likelihood principle.  In: Petrov, B.N. & Csaki, F. (Eds.), Proceedings of the 2nd International Symposium on Information theory, bn petrow, f. Czaki, Akademiai Kiado, Budapest, pp. 267–281.
    Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22 (3), 148–155. https://doi.org/10.1016/j.tree.2006.11.004
    Bouché, M.B. (1972) Lombriciens de France. Ecologie et systématique, Vol. 72, No. HS. INRA Editions, Paris, 671 pp.
    Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540–552 https://doi.org/10.1093/oxfordjournals.molbev.a026334
    Csuzdi, C., Pop, V.V. & Pop, A.A. (2011) The earthworm fauna of the Carpathian Basin with new records and description of three new species (Oligochaeta: Lumbricidae). Zoologischer Anzeiger-A Journal of Comparative Zoology, 250 (1), 2–18. https://doi.org/10.1016/j.jcz.2010.10.001
    Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9 (8), 772. https://doi.org/10.1038/nmeth.2109
    Decaëns, T., Porco, D., Rougerie, R., Brown, G.G. & James, S.W. (2013) Potential of DNA barcoding for earthworm research in taxonomy and ecology. Applied Soil Ecology, 65, 35–42. https://doi.org/10.1016/j.apsoil.2013.01.001
    Decaens, T., Porco, D., James, S.W., Brown, G.G., Chassany, V., Dubs, F., ... & Roy, V. (2016). DNA barcoding reveals diversity patterns of earthworm communities in remote tropical forests of French Guiana. Soil Biology and Biochemistry, 92, 171–183. https://doi.org/10.1016/j.soilbio.2015.10.009
    Gunnell, Y., Calvet, M., Brichau, S., Carter, A., Aguilar, J.P. & Zeyen, H. (2009) Low long-term erosion rates in high-energy mountain belts: Insights from thermo-and biochronology in the Eastern Pyrenees. Earth and Planetary Science Letters, 278 (3–4), 208–218. https://doi.org/10.1016/j.epsl.2008.12.004
    Haldane, J.B. (1926) On being the right size. Harper’s Magazine, 152, 424–427.
    Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic acids symposium series, 41 (1), 95–98.
    Hebert, P.D., Ratnasingham, S. & De Waard, J.R. (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London, Series B: Biological Sciences, 270 (suppl 1), S96–S99. https://doi.org/10.1098/rsbl.2003.0025
    Hernández-Triana, L.M., Prosser, S.W., Rodríguez-Perez, M.A., Chaverri, L.G., Hebert, P.D.N. & Ryan Gregory, T. (2014) Recovery of DNA barcodes from blackfly museum specimens (D iptera: S imuliidae) using primer sets that target a variety of sequence lengths. Molecular Ecology Resources, 14 (3), 508–518. https://doi.org/10.1111/1755-0998.12208
    Katoh, K., Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. https://doi.org/10.1093/molbev/mst010
    Lavelle, P., Decaëns, T., Aubert, M., Barot, S., Bureau, F., Margerie, P., Mora, P. & Rossi, J.P. (2006) Soil invertebrates and ecosystem services. European Journal of Soil Biology, 42, suppl. 1, S3–S15. https://doi.org/10.1016/j.ejsobi.2006.10.002
    Lavelle, P., Spain, A., Blouin, M., Brown, G., Decaëns, T., Grimaldi, M., Jiménez, J.J., McKey, D., Mathieu, J., Velasquez, E. & Zangerlé, A. (2016) Ecosystem engineers in a self-organized soil: A review of concepts and future research questions. Soil Science, 181 (3/4), 91–109. https://doi.org/10.1097/SS.0000000000000155
    Marchán, D.F., Novo, M., Fernández, R., De Sosa, I., Trigo, D. & Cosín, D.J.D. (2016a) Evaluating evolutionary pressures and phylogenetic signal in earthworms: a case study-the number of typhlosole lamellae in Hormogastridae (Annelida, Oligochaeta). Zoological Journal of the Linnean Society, 178 (1), 4–14. https://doi.org/10.1111/zoj.12410
    Marchán, D.F., Sánchez, N., Novo, M., Fernández, R., Pardos, F. & Cosín, D.J.D. (2016b) Cryptic characters for cryptic taxa: On the taxonomic utility of the genital chaetae in earthworms (Oligochaeta, Hormogastridae). Zoologischer Anzeiger-A Journal of Comparative Zoology, 264, 17–28. https://doi.org/10.1016/j.jcz.2016.06.008
    Marchán, D.F., Fernández, R., de Sosa, I., Sánchez, N., Cosín, D.J.D. & Novo, M. (2018a) Integrative systematic revision of a Mediterranean earthworm family: Hormogastridae (Annelida, Oligochaeta). Invertebrate Systematics, 32 (3), 652–671. https://doi.org/10.1071/IS17048
    Marchán, D.F., Fernandez, R., Sanchez, N., Sosa, I.D., Díaz Cosín, D.J. & Novo, M. (2018b) Insights into the diversity of Hormogastridae (Annelida, Oligochaeta) with descriptions of six new species. Zootaxa, 4496 (1), 65–95. https://doi.org/10.11646/zootaxa.4496.1.6
    Marchan, D.F., Decaens, T., Cosin, D.J.D., Hedde, M., Lapied, E. & Domínguez, J. (2020) French Mediterranean islands as a refuge of relic earthworm species: Cataladrilus porquerollensis sp. nov. and Scherotheca portcrosana sp. nov. (Crassiclitellata, Lumbricidae). European Journal of Taxonomy, 701. https://doi.org/10.5852/ejt.2020.701
    Marchán, D.F., Csuzdi, C., Decaëns, T., Szederjesi, T., Pizl, V. & Domínguez, J. (2021) The disjunct distribution of relict earthworm genera clarifies the early historical biogeography of the Lumbricidae (Crassiclitellata, Annelida). Journal of Zoological Systematics and Evolutionary Research, 59, 1703–1717. https://doi.org/10.1111/jzs.12514
    Michaelsen, W. (1900) Die Lumbriciden-Fauna Eurasiens. Annuaire du Museum de St.-Petersburg, 5, 213–225.
    Michaelsen, W. (1925) Regenwürmer aus dem nordlichen und ostlichen Spanien. Senckenbergiana, Frankfurt-a-Main, 7, 186–195.
    Miller, M.A., Pfeifferm, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In 2010 gateway computing environments workshop (GCE), Ieee, pp. 1–8. https://doi.org/10.1109/GCE.2010.5676129
    Novo, M., Almodóvar, A., Fernández, R., Giribet, G. & Díaz Cosín, D.J. (2011) Understanding the biogeography of a group of earthworms in the Mediterranean basin—The phylogenetic puzzle of Hormogastridae (Clitellata: Oligochaeta). Molecular Phylogenetics and Evolution, 61 (1), 125–135. https://doi.org/10.1016/j.ympev.2011.05.018
    Novo, M., Almodóvar, A., Fernández, R., Trigo, D., Díaz-Cosín, D.J. & Giribet, G. (2012) Appearances can be deceptive: different diversification patterns within a group of Mediterranean earthworms (Oligochaeta, Hormogastridae). Molecular Ecology, 21, 3776–3793. https://doi.org/10.1111/j.1365-294X.2012.05648.x
    Pop, V. (1947) Lombriciens de la Corse. Archives de Zoologie expérimentale et générale, 85, 18.
    Qiu, J.P. & Bouché, M.B. (1998a) Révision des taxons supraspécifiques de Lumbricoidea. Documents pédozoologiques et intégrologiques, 3, 179–216.
    Qiu, J.P. & Bouché, M.B. (1998b) Contribution to the taxonomy of Hormogastridae (Annelida: Oligochaeta) with description of new species from Spain. Documents pèdozoologiques et intégrologiques, 4 (15), 164–177.
    Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, syy032.  https://doi.org/10.1093/sysbio/syy032
    Ratnasingham, S. & Hebert, P.D.N. (2007) bold: the barcode of life data system (http:// www.barcodinglife.org). Molecular Ecolology Notes, 7, 355–364. https://doi.org/10.1111/j.1471-8286.2007.01678.x
    Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61 (3), 539–542. https://doi.org/10.1093/sysbio/sys029
    Rota, E. (1993) Contribution to the taxonomy of the Hormogastridae (Annelida: Oligochaeta) with description of two new species from southern France. Journal of Natural History, 28 (1), 27–36. https://doi.org/10.1080/00222939400770031
    Schwarz, G. (1978) Estimating the dimension of a model. The annals of statistics, 6 (2), 461–464. https://doi.org/10.1080/00222939400770031
    Suc, J.P. & Fauquette, S. (2012) The use of pollen floras as a tool to estimate palaeoaltitude of mountains: the eastern Pyrenees in the Late Neogene, a case study. Palaeogeography, Palaeoclimatology, Palaeoecology, 321, 4–54.
    https://doi.org/10.1016/j.palaeo.2012.01.014
    Suchard, M.A., Lemey, P., Baele, G., Ayres, D.L., Drummond, A.J. & Rambaut, A. (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evolution, 4 (1), vey016. https://doi.org/10.1093/ve/vey016
    Turbé, A., De Toni, A., Benito, P., Lavelle, P., Lavelle, P., Ruiz, N., Van der Putten, W.H., Labouze, E. & Mudgal, S. (2010) Soil biodiversity: functions, threats and tools for policy makers. Bio Intelligence Service, Paris, 249 pp. [Report for European Commission (DG Environment)

  2.